Abnormal social reward processing in autism as indexed by pupillary responses to happy faces

Creators: Sepeta, Leigh; Tsuchiya, Naotsugu; Davies, Mari S.; Sigman, Marian; Bookheimer, Susan Y.; Dapretto, Mirella

Abstract

Background: Individuals with Autism Spectrum Disorders (ASD) typically show impaired eye contact during social interactions. From a young age, they look less at faces than typically developing (TD) children and tend to avoid direct gaze. However, the reason for this behavior remains controversial; ASD children might avoid eye contact because they perceive the eyes as aversive or because they do not find social engagement through mutual gaze rewarding. Methods: We monitored pupillary diameter as a measure of autonomic response in children with ASD (n = 20, mean age = 12.4) and TD controls (n = 18, mean age = 13.7) while they looked at faces displaying different emotions. Each face displayed happy, fearful, angry or neutral emotions with the gaze either directed to or averted from the subjects. Results: Overall, children with ASD and TD controls showed similar pupillary responses; however, they differed significantly in their sensitivity to gaze direction for happy faces. Specifically, pupillary diameter increased among TD children when viewing happy faces with direct gaze as compared to those with averted gaze, whereas children with ASD did not show such sensitivity to gaze direction. We found no group differences in fixation that could explain the differential pupillary responses. There was no effect of gaze direction on pupil diameter for negative affect or neutral faces among either the TD or ASD group. Conclusions: We interpret the increased pupillary diameter to happy faces with direct gaze in TD children to reflect the intrinsic reward value of a smiling face looking directly at an individual. The lack of this effect in children with ASD is consistent with the hypothesis that individuals with ASD may have reduced sensitivity to the reward value of social stimuli.

Additional Information

© 2012 Sepeta et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received: 3 February 2012 Accepted: 7 June 2012 Published: 7 June 2012. This work was supported in part by grants from the National Institute of Child Health and Human Development (PO1 HD035470) and Autism Speaks. NT was supported by the Japan Science and Technology Agency and Japan Society for the Promotion of Science, as well as NIMH grant MH080721 awarded to Ralph Adolphs. The contents of this study are solely the responsibility of the authors and do not necessarily represent the official views of NICHD. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank Dan Kennedy and Ashley Scott for their comments on an earlier version of this manuscript. Funding for this proposal and investigators was provided by: NICHD: 1P50 HD055784 (Bookheimer, Dapretto, Sepeta); Japan Science and Technology Agency and Japan Society for the Promotion of Science (Tsuchiya). Authors' contribution: SYB, MD and MSD contributed to the creation of the experimental design. MSD created the stimuli using Adobe Photoshop. LS acquired the data. NT and LS performed the data analyses and jointly wrote the paper. All authors discussed the results, agreed with the interpretation of the findings, and contributed to the writing and editing of the manuscript. All authors read and approved the final manuscript.

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